Primate Sociality and Social Systems

Many primates and other animals live in social groups. In social groups, individual members coordinate their activities, communicate with one another, and interact in both affiliative (friendly) and agonistic (aggressive or submissive) ways. In many social groups, individuals are gregarious; that is, they interact with one another frequently, engage in a variety of types of social interactions, and typically form and maintain social bonds (strong social relationships) with other individuals (Dunbar 1988, Silk 2007). These bonds are often expressed in the form of grooming, a common social activity among primates in which one individual carefully picks through the fur of another and removes any debris or ectoparasites (Figure 1). Grooming serves an important social function for most primates in addition to its hygienic function (Henzi & Barrett 1999).

Group life carries with it inevitable conflict and competition. Individuals must share food resources, water resources, sleeping sites, and mates. While usually mediated by dominance hierarchies in which higher-ranking individuals have priority of access to limited resources, aggressive competition over food and mates is common in primates, and is not only energetically costly but can lead to injury and even death (Mason & Mendoza 1993). In addition to energy costs and risk of injury, high levels of aggression-given or received-can lead to chronic psychological stress. Chronic stress can adversely affect health and reproduction in numerous ways (Sapolsky 2002). Other socially-induced events may also increase stress levels: in chacma baboons, for example, infanticidal (infant killing) behavior by males-or even simply the immigration of a potentially infanticidal male into a social group-increases stress hormone levels in females with infants (Engh et al. 2006). In addition to these social costs of group living, close social contact also increases the potential transmission of pathogens, which increases each individual's risk of contracting infectious diseases. Finally, groups may be disadvantageous because they are more easily detectable by predators compared to solitary individuals.

Given all of these potential costs of group living, why do so many primates-and other mammals-bother living in groups at all? One might especially wonder about this for the lowest-ranking individuals in a social group (i.e., those who are last in line for the available resources).

Despite the costs, sociality is important to these animals for several reasons. Probably most importantly, living in a group likely decreases one's risk of falling victim to predation (van Schaik 1983). There are three reasons for this. First, in social groups there are more individuals looking out for predators and thus predators will be detected more quickly. Second, living in a group decreases each individual's chance of being preyed upon due to an effect called "geometry for the selfish herd" (Hamilton 1971): this states that the larger the group (e.g., 100 versus 10), the lower each individual's chance (1/100 versus 1/10) of becoming prey. Third, individuals in groups can collectively mob predators and successfully drive them away, whereas lone individuals cannot.

Sociality also benefits animals via access to food and other resources. In groups, there are many individuals looking for food simultaneously and thus detection of good food resources (e.g., ripe fruit; Figure 2) will inevitably be communicated to others simply because group members are usually in close proximity to one another. Group members will also benefit from cooperation over defense of food-or other limited resources such as water holes and sleeping sites-as groups can out-compete individuals, and larger groups can out-compete smaller groups (Wrangham 1980).

In addition, sociality is beneficial to group-living animals in that it makes it easier for them to find mates. Animals that do not live in groups must either search for mates or opportunistically mate when they encounter other individuals. Group-living animals simply choose mates within their social group.

Moreover, sociality allows cooperative socialization of offspring. In social groups, infants and juveniles play with one another, which develops motor skills as well as the social skills necessary to survive and reproduce in a social setting. For example, during social play juveniles receive reinforcement from adults about how dominance hierarchies work, and what it means to have a given rank within a social group of a given species. Thus when they reach adulthood they will have learned what they can and cannot do, and thereby fit into the social fabric of their social group (Pereira & Fairbanks 1993).

Finally, sociality in and of itself appears to carry benefits for individuals. As noted above, one of the costs of group living is the potentially high level of conflict and aggression that occurs among group members, which involves greater energy expenditure, risk of injury, and chronic stress. In baboons, this socially-induced stress appears to be alleviated by the receipt of affiliative vocalizations, as well as the maintenance of grooming relationships with a small network of close associates (Crockford et al. 2008). Ultimately, female baboons with strong social bonds (i.e., social relationships characterized by frequent proximity and grooming; Figure 3) experience greater offspring survival and even longer lifespans than females with weaker bonds (Silk et al. 2003, 2009, 2010). These studies demonstrate that strong social relationships within groups, beyond group living alone, can carry important fitness benefits for individuals.

The social system of a given species is an outcome of (1) its social structure, the size and composition of a typical group of that species, and (2) its social organization, how those individuals are organized (i.e., the patterns of spacing, agonistic and affiliative social interactions, philopatry [whether one or both sexes remain in their natal group], and dispersal [whether one or both sexes move to a new group to reproduce]) that typify that species. Each species also tends to have a characteristic mating system (i.e., the pattern of mating among members of each sex). All of these aspects of primate societies vary widely across the primate order.

The least gregarious primates have what is often referred to as a solitary dispersed social system. In these primates, an adult male's territory overlaps the territory of one or more adult females, but each individual forages alone and maintains social contact mainly through vocal and/or olfactory communication. These primates are typically nocturnal, foraging at night and sleeping in trees during the day. The mating system in these primates is usually polygynous (i.e., each male mates with multiple females). This type of social system characterizes galagos, lorises, some lemurs, some tarsiers, and orangutans. Notably, orangutans are the only anthropoid primates with a solitary social system.

Titi monkeys, owl monkeys, some callitrichids (marmosets and tamarins), and many hylobatids (gibbons and siamangs) are characterized by a pair-bonded social system. Here, one adult male and one adult female form a small social group and defend a territory from other pairs. The mating system in these groups is usually monogamous (only one male mates with only one female), though extra-pair copulations have been observed (Palombit 1994), and the male usually participates in offspring care, which is unusual for male mammals (Fuentes 2002).

Many marmosets and tamarins live in one-female multi-male groups characterized by cooperative breeding. In this type of system, usually only one female breeds, and that female suppresses the reproduction of any subordinate females via aggression and/or pheromonal (olfactory) signals. Usually there is more than one breeding male, thus the mating system is polyandrous, a rarity among mammals. Some or all of the individuals in these groups participate in offspring care and this social system is thus often called cooperative polyandry.

One of the most common primate social systems is the one-male group, which characterizes most colobine monkeys, most guenons, patas monkeys, howler monkeys, and some gorillas. Here, a single resident adult male defends a group of (usually) philopatric, related females from other males and, while his tenure lasts, enjoys exclusive mating access to those females (i.e., polygyny). Sometimes called harems, these groups are always at risk of takeover by non-resident males, who typically form all-male groups while awaiting their chance to become a resident male. Often, takeovers are accompanied by infanticide, in which the new resident male kills the young infants in the group. This behavior has the effect of bringing the mothers back into estrus (sexual receptivity) sooner than they would have otherwise.

Also common among primates are multi-male multi-female groups, in which multiple individuals of each sex form large social groups in which the mating system is usually polygynandrous (i.e., both males and females are polygamous in that they mate with multiple members of the opposite sex). These are the largest groups of primates, and usually quite complex socially, with differentiated social and kin relationships among group members. This type of social system characterizes many monkeys, including macaques, most baboons, vervet monkeys, mangabeys, capuchins, squirrel monkeys, woolly monkeys, and some colobine monkeys, as well as some lemurs-most notably the ringtailed lemur and sifaka. In most of these species, females are philopatric and males disperse.

Similar to multi-male multi-female groups are the fission-fusion communities of chimpanzees, bonobos, spider monkeys, and some other ateline monkeys. Fission-fusion communities are less cohesive than typical multi-male multi-female groups. These groups occupy very large home ranges in which temporary foraging parties cleave and coalesce over time with changes in resource availability and female reproductive condition. These social systems are typically characterized by female dispersal and male philopatry.

The most complex type of social system found in primates, and in mammals as whole, is the multi-level society (also known as a hierarchical or modular society) characterizing hamadryas baboons (Figure 4), geladas, snub-nosed monkeys, and a few other mammals such as elephants. In this type of system, there are at least three levels of social structure: the one-male unit (OMU), the band, and the troop or herd. The OMU is the reproductive unit and consists of one "leader" male, sometimes a follower male, and several females; the band is the ecological unit that forages and sleeps together, and the troop or herd is a temporary aggregation at a sleeping site or foraging area. In hamadryas baboons, there is a fourth layer between the OMU and the band, the clan, which consists of OMUs and bachelor males linked by social bonds and possibly kinship among males. In geladas, bachelor males join together to form all-male groups. Reproduction in these societies is usually polygynous, and OMUs are always at risk of takeover by bachelor males, who may commit infanticide after taking over females with young infants.

It is important to note that the social organization of a species might not be immediately apparent from its social structure. For example, both geladas (Figure 1) and hamadryas baboons (Figure 4) are characterized by multiple layers of society, and their social structure is almost identical. However, the social organization of these two species could not be more different (Kummer 1967, Dunbar 1983). In geladas, cohesion of OMUs is maintained by philopatric females, as each OMU is a female kin group and these kin groups are taken over as entire units by males. In hamadryas, by contrast, cohesion of OMUs is maintained by philopatric males who take over females one by one, often exchanging them with other males in their clans (Pines et al. 2011), and aggressively condition those females to remain in their OMU. Thus, hamadryas social organization includes strong male-female bonds (the glue that holds together an OMU) and strong male-male bonds (as males are philopatric and thus related to one another within bands and clans), whereas gelada social organization is characterized by strong female-female bonds (which hold together OMUs) but weak bonds between the sexes.

Moreover, one must be careful not to make assumptions about a species' mating system simply upon observing its social system. For example, multi-male multi-female groups of gorillas may have an age-graded dominance structure in which only the oldest, highest-ranking (alpha) silverback male is allowed to copulate; in this case, the mating system is not polygynandrous (as one might expect in a multi-male group) but instead polygynous (Robbins 2011). Another example can be found in guenons, which live in one-male groups. During the mating season multi-male influxes occur in which outside males come into the group, copulate with the females, and then leave again (Cords 1988). The mating system in this case is not polygynous, which one would expect, but polygynandrous. Finally, gibbons and siamangs were first thought to be monogamous, but then observations of extra-pair mating (i.e., copulations with individuals outside of the pair-bond) confirmed that they are not always monogamous but sometimes polygynous, polyandrous, or both (Palombit 1994).